View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Dartmouth Digital Commons (Dartmouth College) Dartmouth College Dartmouth Digital Commons Dartmouth Faculty Open Access Articles Open Dartmouth: Faculty Open Access 11-1-2014 Publication trends in model organism research Michael Dietrich Dartmouth College Rachel Ankeny University of Adelaide Patrick Chen Dartmouth College Follow this and additional works at: http://digitalcommons.dartmouth.edu/facoa Part of the Biology Commons, and the Plant Sciences Commons Recommended Citation Dietrich, Michael; Ankeny, Rachel; and Chen, Patrick, "Publication trends in model organism research" (2014). Dartmouth Faculty Open Access Articles. 5. http://digitalcommons.dartmouth.edu/facoa/5 This Article is brought to you for free and open access by the Open Dartmouth: Faculty Open Access at Dartmouth Digital Commons. It has been accepted for inclusion in Dartmouth Faculty Open Access Articles by an authorized administrator of Dartmouth Digital Commons. For more information, please contact [email protected]. HIGHLIGHTED ARTICLE PERSPECTIVES Publication Trends in Model Organism Research Michael R. Dietrich,*,1 Rachel A. Ankeny,† and Patrick M. Chen* *Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755 and †School of History and Politics, The University of Adelaide, Adelaide, South Australia 5005, Australia ABSTRACT In 1990, the National Institutes of Health (NIH) gave some organisms special status as designated model organisms. This article documents publication trends for these NIH-designated model organisms over the past 40 years. We find that being designated a model organism by the NIH does not guarantee an increasing publication trend. An analysis of model and nonmodel organisms included in GENETICS since 1960 does reveal a sharp decline in the number of publications using nonmodel organisms yet no decline in the overall species diversity. We suggest that organisms with successful publication records tend to share critical characteristics, such as being well developed as standardized, experimental systems and being used by well-organized communities with good networks of exchange and methods of communication. Y the end of the 20th century, “model organisms” were Some model organisms were selected because a certain Bone of the centerpieces of biomedical research. Or so subsystem or process was particularly accessible in the given goes the usual narrative (Davis 2004). The historical origins species, such as the development of the nervous system in of the term model organism are difficult to trace, but it is the nematode Caenorhabditis elegans (de Chadarevian 1998; clear that the concept of a model organism took a firm hold Ankeny 2000, 2001b); others because techniques and infor- in the 1960s and 1970s in part due to the rise of the techni- mation were already available from previous research work, ques of molecular biology. The development of experimental for example, Drosophila melanogaster (Kohler 1994; Weber systems around organisms, such as Drosophila, mice, and 2007), various mouse and rat strains (Rader 2004; Logan maize, has an even longer history in genetic research (Kohler 2002, 2005; Leonelli et al. 2014); and still others such as 1994; Rader 2004), and it is defensible to claim that the zebrafish were chosen explicitly to be developed in detail concepts associated with model organisms long predate the although they had not previously been extensively studied actual use of the terminology. Contemporary model organ- (Grunwald and Eisen 2002). The criteria usually cited as isms tend to be species (or, more precisely, strains of these justifying the use of some species as a model organism in- species) that are relatively simple and hence experimentally clude a rapid life cycle that permits the growth of large tractable. They were developed as resource materials in order populations in short periods of time and increases the likeli- to study particular biological phenomena exhaustively or in hood of spontaneous genetic mutations, relatively simple great detail, usually including genetic and developmental reproductive cycles and genomes, and relatively small body processes. Although in many cases the organism under study sizes and physical robustness under laboratory conditions, was of interest in its own right to those who did research with such that large, standardized populations can be bred and it, the underlying expectations were that discoveries made in maintained. A wide range of organisms were utilized to in- these organisms would be useful or in some sense applicable vestigate fundamental biological processes during the 20th for understanding other organisms, including humans, or century, but it was not until the planning and implementa- even fundamental mechanisms shared by many or all living tion of the genome mapping and sequencing projects of the entities. (For an overview of this history and of the concept of 1990s that a canonical set of model organisms was named a model organism, see Ankeny and Leonelli 2011, as well as by the National Institutes of Health (NIH)for biomedical re- earlier commentaries in Gest 1995; Ankeny 2001a.) search (NIH 1999). The designation of a relatively limited set of organisms as Copyright © 2014 by the Genetics Society of America model organisms by the NIH has proven controversial in doi: 10.1534/genetics.114.169714 1Corresponding author: Department of Biological Sciences, Dartmouth College, some quarters. For instance, critics argue that many of these Hanover, New Hampshire 03755. E-mail: [email protected] model organisms were chosen without attention to phylogenetic Genetics, Vol. 198, 787–794 November 2014 787 similarities and based on assumptions of conservation of assume that what was included in these databases reflected various processes that were not warranted given the avail- what the community considered to be “its” research. Within able evidence. They question the built-in assumptions of these databases, we excluded a range of publications that we universality (or near universality), which they claim led to concluded did not fit the conventional definition of research, a lack of focus on variation and relatively little comparative including abstracts, dissertations, personal communication, work, as well as limitations on the study of development in it supplemental material, letters, poems, book reviews, and se- own right as well as in the context of evolution (e.g., Bolker quence accessions. We are well aware that publishing norms 1995, 2012; Gest 1995; Jenner and Wills 2007; Gilbert may differ from community to community, and it was impos- 2009; Sedivy 2009; Sommer 2009; for a historical perspec- sible to control for differential community norms in terms of tive, see Laubichler and Geison 2001). Further, the very pro- the types of data published, the frequency with which inves- cesses that contribute to the standardization of model tigators published, the quantity of data published (e.g.,all organisms within the laboratory, in fact, may render them articles regardless of length and content were counted as insensitive to environmental variation and hence atypical in the same), data held back or only published electronically, a problematic sense. Therefore, these skeptics censure re- and so on. However, it quickly became apparent that different search centered on model organisms for placing undue empha- databases used different procedures for collecting publication sis on molecular-level processes and paying inadequate data and that a variety of types of publications were included. attention to higher-level environmental and other epige- C. Robertson McClung published a publication chart that one netic factors. In addition, disputes have occurred between of us (M.R.D.) prepared for Drosophila, Arabidopsis, maize, the communities who work on particular model organisms and rice using the research articles collected in databases for as to what constitutes success or effectiveness in model each organism: Drosophila,FlyBase,http://www.flybase.org; organism research. Members of the wider biological com- Arabidopsis,TheArabidopsis Information Resource, http:// munity, particularly those who do not work on one of the www.arabidopsis.org/index.jsp; maize, Maize Genetics and NIH-designated model organisms, have complained about Genomics Database, http://www.maizegdp.org/; rice, Oryza- the “swamping out” of basic biological research due to the base, http://www.shigen.nig.ac.jp/rice/oryzabase/top/ funneling of grant monies into research on these organisms top.jsp (McClung 2008a,b). However, MaizeGDB and the (cf. Davies 2007, whose analysis shows no dominance of Maize Genetics Executive Committee (2008) responded that particular organisms within certain publications in devel- the data on maize underestimated maize publications be- opmental biology), while advocates of model organism cause they had stopped curating publications in 2003. The approaches (e.g., Ledford 2010) note that continued fund- rice data were also reported to be an underestimate. ing is necessary to achieve the long-term goals inherent in McClung withdrew both maize and rice from the figure in this type of research. the online ASPB News (MaizeGDB and the Maize Genetics Against the backdrop of this history, we set out to analyze Executive Committee 2008). publication trends in biological research using the organisms Moreover, curatorial standards for references in these